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Home , Desert night lizard, Island night lizard, Lizard, Night lizard, Teiidae, Xantusia

Divergence in the Island Night riversiana (: Xantusiidae)

R. L. Bezy,1 G. C. Gorman,2 G. A. Adest,2 and Y. J. Kim2 1Section of Herpelology, Los Angeles County Museum of Natural History, Los Angeles, California 90007 2Department of Biology, University of California, Los Angeles, California 90024

INTRODUCTION The island , Xantusia riversiana Cope (Fig. 1), is found only on Santa Barbara, San Clemente, and San Nicolas Islands off southern California (Fig. 2). The is sufficiently divergent in morphology from its mainland relatives, X. vigilis Baird and X. henshawi Stejneger (Fig. 1), that it has been placed in the monotypic Klauberina by Savage (1957, 1963). Regardless of whether it is accorded generic (Savage 1957) or subgeneric (Bezy 1972) rank, X. riversiana is clearly more divergent than the other living of the California Channel Islands, suggesting that it may have been present longer than other species on one or more of the islands. Moreover, casual observations indicate that there may be greater morphological differences between the island populations of X. riversiana than were documented by earlier work (Savage 1951, Smith 1946). In an effort to further clarify the evolutionary history of the species, we have compared electrophoretically determined genetic- distances and divergence time estimates between the island populations with those between the species of Xantusia, and have reappraised inter-island differences in karyotypes, scalation, coloration, body size, clutch size, and variability.

MATERIALS AND METHODS Two separate electrophoretic analyses were performed. In the first, 22 presumptive loci were scored for 15 X. riversiana from San Clemente Island, 15 from San Nicolas Island, and five from Santa Barbara Island. In the second study, 30 presumptive loci were analyzed for six X.. riversiana from San Nicolas Island, six X. riversiana from San Clemente Island, six X. henshawi from the San Jacinto Mountains, and 20 X. vigilis from Antelope Valley, California (see Specimens Examined for exact localities). The procedures for preparing the gels, stains, and interpreting alleles follow Selander et al. (1971), with minor modifications (Yang et al. 1974, Kim et al. 1976). The chromosomal methods utilized were described by Bezy (1972). Scalation was analyzed univariately with the BMDP3D program and multivariately by stepwise discriminant analysis (SDA) utilizing BMDP7M (Dixon 1975).

RESULTS Electrophoresis The 22-locus study indicated that 18 presumptive loci are fixed for identical electromorphs (alleles) in all three island samples. Polymorphisms were observed for MDH (San Nicolas Island), PGM-2 (San Clemente and Santa Barbara Islands), and GOT-2 and PGI (San Clemente and San Nicolas Islands) (Table i). In the 30-locus study, identical alleles were fixed at 27 loci for San Clemente and San Nicolas; polymorphisms occurred for MDH-2 on San Nicolas and for ADH and PGM-2 on San Clemente (Table 2). Allele frequencies were used to compute genetic- similarity and distance (Nei 1972). Inter-island genetic distances (Table 3) are, of course. 566 DIVERGENCE

FIGURE 1. Living individuals of Xantusia riversiana (upper; San Clemente I.), X. henshawi (middle; LACM 127160; California: Riverside Co.: San Jacinto Mts., Snow Creek), and X. vigilis (lower; LACM 127154; Mexico: Durango: 6.5 mi NE Pedricena).

FIGURE 2. Distribution of Xantusia riversiana (three stippled islands). Arrows indicate specific populations sampled. R. L. BEZY ET Al. 567

TABLE I. Allelic frequencies at four presumed loci for three island populations of Xantusia riversiana. Excluded are 18 presumed loci fixed for electrophoretically identical gene products: GP-1. GP-2, GP-3, GP-4, LDH-1, LDH-2, IDH-1, IDH-2, ADH, Pept-1, Pept-2 ES GOT-I PGM-1, MP1, XDH, SDH, and IPO.

Island population (Sample size)

Locus Allele San Clemente (15) San Nicolas (15) Santa Barbara (5)

MDH a 0 .067 0 b 0 .033 0 c 1.0 .900 1.0 PGI a .033 .036* 0 b .967 .964 1.0 GOT-2 a .067 .033 0 b .933 .967 1.0 PGM-2 a .167 0 .2 b .833 1.0 .8

* Sample size = 14.

extremely small, since identical alleles either predominate or are fixed at all of the loci studied electrophoretically. While genetic distance values are smallest between Santa Barbara and San Clemente Islands (0.0004) and largest between San Nicolas and Santa Barbara Islands (0.0024; Table 3), none differ significantly from zero. Xantusia riversiana was compared with X. vigilis and X. henshawi in the 30-locus study (Tables 2 and 3). Fixed differences occur between X. riversiana and X. vigilis at 10 loci (Nei distance, ND = 0.574), between X. riversiana and X. henshawi at 14 loci (ND = 0.830), and between the two mainland species at 8 loci (ND = 0.409).

Karyotypes The chromosomes of from Santa Barbara (1 female, 34 cells) and San Nicolas (1 male,5 3 cells) appear identical in number, shape, and relative size to those described by Bezy (1972) for the population on San Clemente (Fig. 3). Utilizing nonbanding techniques, this karyotype also appears identical to that of eastern populations of X. vigilis and X. henshawi (Bezy 1972).

Scalation From a total of 217 specimens, data were taken for the following seven characters: scales around body (SAB; transverse count of dorsal scales at midbody); gulars (G; longitudinal count along ventral midline from gular fold to postmentals); fourth toe lamellae (FTL; longitudinal count, ventral midline); femoral pores (FP; one leg); ventrals (V; longitudinal count along midline, excluding preanals); preanals (PA; number of enlarged scales along midline between vent and ventrals); preanal enlargement (PAE; sum of diameters of four largest preanals over sum of lengths of four midbody ventrals). These characters were chosen because previous studies suggest they vary geographically in species of Xantusia (Bezy 1967, Smith 1946, Webb 1970). was not significant (P ≥ 0.05) in the largest sample (San Clemente, NW, mottled; 20 male,2 0 female). and the sexes were combined in subsequent analyses. Univariate analysis indicates significant (P < 0.05) differences between islands for all seven characters, except for ventrals and preanals between Santa Barbara and San Clemente Islands (Table 4). Stepwise discriminant analysis indicates significant separation between island 568 ISLAND NIGHT LIZARD DIVERGENCE

TABLE 2. Allelic frequencies at 18 presumed loci for four populations of Xantusia. Excluded are 12 loci that were fixed identically in all four populations: LDH-1, LDH-2, IDH-1, IDH-2, aGPDH, MP1, PGI, IPO-1, FUM, LAP, AB-2, and AB-3.

Species, Population, Sample size

riversiana riversiana henshawi vigilis San Nicolas San Clemente San Jacinto Little Rock Locus Allele 6 6 6 20

MDH-1 a 0 0 1.0 1.0 b 1.0 1.0 0 0 MDH-2 a .167 0 1.0 1.0 b .833 1.0 0 0 6PGDH a 1.0 1.0 .083 0 b 0 0 .917 1.0 XDH a 0 0 1.0 0 b 1.0 1.0 0 0 c 0 0 0 1.0 ADH a 1.0 .917 0 0 b 0 .083 0 0 c 0 0 1.0 0 d 0 0 0 1.0 SDH a 0 0 1.0 0 b 1.0 1.0 0 1.0 PGM-1 a 0 0 1.0 1.0 b 1.0 1.0 0 0 PGM-2 a 0 0 .25 .5 b 0 .33 .75 .5 c 1.0 .67 0 0 Pept-1 a 0 0 1.0 1.0 b 1.0 1.0 0 0 ME a 0 0 1.0 1.0 b 1.0 1.0 0 0 HEXO a 0 0 1.0 0 b 1.0 1.0 0 1.0 AB-1 a 1.0 1.0 0 1.0 b 0 0 1.0 0 ES-1 a 0 0 1.0 .9 b 1.0 1.0 0 .1 ES-2 a 0 0 0 .925 b 0 0 1.0 .075 c 1.0 1.0 0 0 ES-3 a 1.0 1.0 0 1.0 b 0 0 1.0 0 1PO-2 a 0 0 0 1.0 b i.O 1.0 i.O 0 ES-4 a 0 0 1.0 0 b 1.0 1.0 0 1.0 . R. L. BEZY ET Al 569 TABLE 4. Data for seven scale characters in nine samples of Xantusia riversiana. Mean ± standard error (top line), range (middle Vine), coefficient, of variation (bottom line), and sample size (below population) for scales around body (SAB), gulars (G), fourth toe lamellae (FTL), femoral pores (FP), ventrals (V), preanals (PA), and preanal enlargement (PAE) are given.

SAB G FTL FP V PA PAE

Santa Barbara I. 84.15 ±.48 50.47 ±.46 23.28 ±. 06 11.23 ±.09 34.00 ±..1 6 4.98 ±.10 123.64 ±.2.29 40 79-92 43-58 22-25 10-12 32-37 4-6 105-167 3.64 5.71 4.29 5.14 2.98 13.26 11.71 San Clemente I. 79.55 ±.37 46.98 ±.26 22.67 ±. 12 10.50 ±.08 33.67 ±. 10 4.89 ±.07 140.44 ±.1.87 97 70-88 41-54 21-29 9-13 32-36 3-7 98-181 4.57 5.44 5.39 7.66 2.90 13.82 13.08 San Nicolas I. 71.74 ±.37 41.99 ±.26 21.45 ±. 13 10.94 ±.10 32.56 ±. 11 4.49 ±.06 157.79 ±2.30 80 60-79 35-48 19-24 9-13 30-35 3-6 119-226 4.56 5.64 5.29 8.01 3.12 12.78 13.06 San Clemente I. 81.25 ±.79 47.15 ±.69 22.20 ±. 22 10.45 ±.15 33.95 ±. 20 5.00 ±.10 129.80 ±3.25 Pyramid Cove 75-87 43-54 21-24 10-12 33-36 4-6 108-158 20 4.35 6.50 4.52 6.57 2.61 9.18 9.77 Northwest 78.65 ±.40 46.91 ±.30 22.70 ± .17 10.46 ±.13 33.50 ±. 12 4.73 ±.09 148.98 ±2.11 57 70-86 42-52 21-29 9-12 32-36 3-7 114-181 3.81 4.91 5.71 8.10 2.77 15.21 10.74 mottled 79.00 ±.46 47.25 ±.38 22.40 ±..1 5 10.48 ±.14 33.55 ±. 16 4.80 ±.13 148.20 ±2.37 40 72-86 42-52 21-25 9-12 32-36 3-7 122-181 3.70 5.13 4.27 8.37 2.94 16.48 10.12 striped 77.82 ±.75 46.12 ±.44 23.41 ±. 41 10.41 ±.19 33.41 ±. 19 4.59 ±.12 150.82 ±4.49 17 70-81 42-49 21-29 9-11 32-35 4-5 114-175 3.97 3.90 7.25 7.64 2.38 11.06 12.27 San Nicolas I. 70.05 ±.81 41.25 ±.55 21.30 ±. 22 10.50 ±.19 32.30 ±. 18 4.05 ±.09 158.80 ±6.27 Carrier Cove 60-75 35-44 20-23 9-12 31-34 3-5 121-226 20 5.17 5.98 4.59 7.88 2.48 9.73 17.65 Southeast 72.75 ±.47 42.15 ±.33 21.87 ±. 18 11.23 ±.15 32.77 ±. 17 4.60 ±.08 159.10 ±2.67 40 67-79 37-48 20-24 9-13 31-35 4-6 128-214 4.06 5.00 5.20 8.19 3.35 11.86 10.60 572 ISLAND NIGHT LIZARD DIVERGENCE

FIGURE 4. Plot of first two canonical variables separating the three island populations of Xantusia riversiana: (B) Santa Barbara I., 40 specimens: (C) San Clemente I., 97; and (N) San Nicolas I., 80. Population centroids (dots) are surrounded by 95 per cent confidence circles. The first variate (abscissa) represents 95 per cent of the observed variance.

FIGURE 5. Plot of first two canonical variables separating five populations of Xantusia riversiana: Santa Barbara I. (SB); San Clemente I., Pyramid Cove (SCPC) and Northwest (SCNW); and San Nicolas I., Carrier Cove (SNCC) and Southeast (SNSE). Population cen- troids (dots) are surrounded by 95 per cent confidence circles. First variate (abscissa) represents 86 per cent of observed variance; second (ordinate), 7 per cent. See Figure 2 for location of populations. R. I.. BEZY ET Al. 573

TABLE 5. Inter-island comparisons of airline distance in km (AD), Mahalanobis' distance for scaiation (√D2), and genetic distance of Nei, 1972 (ND).

AD √D2 ND

Santa Barbara-San Clemente 77 1.91 .0004 San Clemente-San Nicolas 101 2.95 .0017 San Nicolas-Santa Barbara 49 4.66 .0024

TABLE 6. Pooled standard deviations and canonical variate coefficients, with standardized scores in parentheses, for seven characters in the inter-island stepwise discriminant analysis.

SD I II

SAB 3.403 0.175 (0.596) -0.025 (-0.085) G 2.555 0.155 (0.396) 0.081 (0.207) FTL 1.153 0.220 (0.254) -0.044 (-0.051) FP 0.797 -0.245 (-0.195) 1.116 (0.889) PAE 18.621 -0.010 (-0.186) -0.017 (-0.317) V 1.000 0.180 (0.180) -0.283 (-0.283) PA 0.634 0.029 (0.018) -0.586 (-0.372)

TABLE 7. Classification matrix based on stepwise discriminant analysis of 216 Xantusia riversiana from Santa Barbara (SB), San Clemente (SC), and San Nicolas (SN) Islands.

Number of cases classified into group

Per cent Total correct SB SC SN

SB 39 87.2 34 6 0 SC 97 78.4 16 76 5 SN 80 91.2 0 7 73 Total 216 84.7 50 88 78

centroids (Fig. 4). As with the results of the electrophoretic analyses, the of increasing divergence (Mahalanobis' distance, √D2) was: San Clemente-Santa Barbara (1.91), San Clemente-San Nicolas (2.95), and Santa Barbara-San Nicolas (4.66) (Tables 5 and 6). The a posteriori classification scored 91 percent hits for San Nicolas, 87 percent for Santa Barbara, and 78 per cent for San Clemente. The classification matrix (Table 7) again emphasizes the intermediate position of San Clemente and its relative closeness to Santa Barbara in the discriminant space. To test for intra-island geographic variation, samples were compared from two distant localities on both San Clemente (NW and Pyramid Cove) and San Nicolas (SE and Carrier Cove) (Fig. 2). Significant differences were found for SAB and PAE between the San Clemente populations, and for SAB, FP. and PA between the San Nicolas populations (Table 4). For both intra-island comparisons the centroids are significantly different (Fig. 5) and their FIGURE 6. Living individuals of Xantusia riversiana from Santa Barbara I. (upper two; LACM 127128 and 108835) and San Clemente I. (lower two; LACM 108618 and 108619). R. L. BEZY ET AL.

FIGURE 7. Living individuals of Xantusia riversiana from San Nicolas I. (LACM 108505 through 108509 and 108813).

Mahalanobis' distances are nearly identical (1.59 and 1.63) and are smaller than for all inter-island comparisons (2.07 to 5.43).

Color Pattern Color pattern in Xantusia riversiana is highly variable (Figs. 6 and 7). Individuals with mottled patterns are found on all three islands; those with longitudinally striped patterns occur on San Clemente and San Nicolas, and a "blank" (uniform tan) pattern was observed only among San Nicolas lizards. There are, however, more subtle island differences in color pattern which we did not attempt to quantify, but which are illustrated in Figures 6 and 7. The color patterns of lizards from San Clemente lend to be more highly contrasting than those of individuals from Santa Barbara (Fig. 6). San Nicolas color patterns are the most variable and include striped, blank, and finely reticulated patterns, as well as many intermediates, often with reddish backgrounds (Fig. 7). Scale counts were compared between striped and mottled individuals in the NW San Clemente population. Significant differences were detected only for fourth toe lamellae. The population centroids do not differ significantly and only 68 per cent hits were scored in the a posteriori classification of the SDA. The apparent association of color morphs with signifi- 576 ISLAND NIGHT LIZARD DIVERGENCE

TABLE 8. Clutch size from two sources for three island populations of Xantusia riversiana. Mean ± standard error, range, and sample size.

Santa Barbara San Clemente San Nicolas

Goldberg and Bezy (1974) 3.50 3.76 ±.23 4.55 ±.50 3-4 2-6 3-7 2 25 9

Brattstrom (1951) — 4.80 ±.37 7.50 ±.65

— 4-6 6-9

— 5 4 Total 3.25* 4.03 ±.20 5.46 ±.55 3-4 2-6 3-9 4 30 13

* Includes two additional individuals (LACM 125466 and 125467), each with three enlarged eggs.

cant differences in FTL may be a result of minor geographic variation, as the NW San Clemente sample was collected over a 6.5-km2 area (Goldberg and Bezy 1974) and local "pockets" of striped individuals were noted in collecting the samples. All three color morphs occur in mainland populations of Xantusia vigilis.

Body Size The means for snout-vent lengths (SVL) of specimens 75 mm or longer (size at maturity for San Clemente females; Goldberg and Bezy 1974) are: Santa Barbara, 83.35 ±1.31 (n = 31); San Ciemente, 84.24 ±0.42 (n = 294); and San Nicolas, 88.85 ±0.80 (n = 86). The differences are significant, except for Santa Barbara vs. San Clemente. Adult Xantusia riversiana (SVL = 65 to 109 mm; Goldberg and Bezy 1974) are considerably larger than their mainland relatives X. vigilis (SVL = 36 to 60 mm; Bezy 1967, Zweifel and Lowe 1966) and X. henshawi (SVL = 47 to 70 mm; Lee 1975) and have been cited as an example of insular gigantism (Carlquist 1965). Large body size may be a primitive character state for xantusiids, retained by X. riversiana, and is perhaps associated with a herbivorous diet (Brattstrom 1952, Mautz and Lopez-Forment 1978, Pough 1973, Regal 1968).

Clutch Size Brattstrom (1951) and Goldberg and Bezy (1974) have presented data on clutch (= litter) size in X. riversiana (Table 8). The figures reported by Brattstrom (1951) are considerably higher than those of Goldberg and Bezy (1974), perhaps reflecting annual variations in clutch size. Clutch size is smallest for Santa Barbara Island and largest for San Nicolas Island in both sets of data, but because of sample size limitations the accepted level of significance is achieved only for San Clemente vs. San Nicolas, and only when the two sets of data are pooled. While a correlation between body size and clutch size was not present in the population on San Clemente (Goldberg and Bezy 1974), it appears to hold for comparisons between island populations. This correlation may also hold for the family in general since clutch size in X. riversiana is clearly larger than in its smaller mainland relatives X. vigilis (X = 1.87; Zweifel and Lowe 1966) and X. henshawi (X = 1.46; Lee 1975), but similar to that of comparably sized species of (4 to 8; Telford and Campbell 1970, Greene 1970). R. L. BEZY ET Al. 577

TABLE. 9. Comparison of eight phenotypic and genotypic characteristics and seven ecogeo- graphical parameters for the three island populations of Xantusia riversiana Color pattern classes are mottled (M), striped (S), and blank (B). Data for last seven parameters (except lizard species number) are from Power (1972).

Santa Barbara San Clemente San Nicolas

Canonical axis I 2.21 0.66 -1.93 Snout-vent length (X, mm) 83.35 84.24 88.85 Clutch size (X) 3.25 3.76 4.55 Color pattern M M, S M, S, B Coefficient of variation (CV1) 4.35 5.19 5.32 Coefficient of variation (CV2) 4.35 4.99 5.19 Heterozygosity (H) 0.9 1.2 1.6 2 Area (km ) 2.6 145 36 Elevation (m) 194 599 253 Latitude (°N) 33.4 32.9 34.0 Mainland distance (km) 61 79 98 Island distance (km) 126 178 150 Plant species number 40 235 190 Lizard species number 1 2 1 ( + 2?)

Variability The mean coefficients of variation (CV) of five scale characters for the island populations are given in Table 9. In computing CV, PA and PAE were not included because of their unusually high level of variability (CV = 13.29 and 12.62, respectively). The order of increasing CV of the island populations is Santa Barbara, San Clemente, and San Nicolas, whether CV for San Nicolas and San Clemente is computed as the average of the CVs of their respective intra-island populations (CV1), or from the pooled standard deviation for the entire island sample (CV2) (Table 9). In comparison with mainland species, X. riversiana does not appear to have reduced scale count variability; CV for four characters (SAB, FTL, G, and FP) in X. vigilis (Bezy 1967) is 5.40, as opposed to 5.47 for X. riversiana. For the 22-locus study, the heterozygosity (H) figures correspond well to CV values, Santa Barbara Island being the least and San Nicolas Island the most variable (Table 3). These data might seem to support the genetic-phenetic variation correlation demonstrated by Soule et al. (1973) for insular Anolis and deep-water island populations of Uta, and by Patton et al. (1975) for Galapagos Rattus. That such a correlation exists for X. riversiana must, however, remain questionable because the number of islands sampled is necessarily limited to three, our electrophoretic sample sizes are small (20, 20, and 5), and the results of the 30-locus study are contradictory, indicating instead that the larger San Clemente is genetically more variable than the smaller San Nicolas. Electrophoretic estimates of genetic variability in the two mainland species are similar to those of the island populations (Table 3). All populations of Xantusia sampled have low heterozygosity values (H =2.21, 30 loci) when compared with other vertebrates (Selander and Kaufman 1973). Gorman et al. (1977) compared heterozygosity estimates for 10 genera of lizards and concluded that the values are low (ca. 2 per cent) in fossorial species, intermediate (ca. 5 per cent) in territorial, sit-and-wait predators, and high (ca. 10 per cent) in vagile. 578 ISLAND NIGHT LIZARD DIVERGENCE

searching predators. These categories presumably influence heterozygosity values through territoriality, population size, and/or mating structure (degree of panmixia). The heterozygosity levels of Xantusia are comparable to those of fossorial species, which these lizards resemble in that they are sedentary, live (often paired) in patchy habitats (e.g., boulder cap rocks and ), and have long lives and low reproductive potentials (Bezy et al. 1977, Goldberg and Bezy 1974, Lee 1975, Zweifel and Lowe 1966).

DISCUSSION Ecological Correlates That our studies of X. riversiana are necessarily limited to three islands precludes any detailed analysis of correlations between the data and island ecological parameters. However, we briefly consider here possible ecological correlates only because a consistent order (Santa Barbara-San Clemente-San Nicolas) occurs in our data for genetic distance, scalation, color pattern, body size, clutch size, heterozygosity, and scale count variability (Table 9). This order contradicts that for island area, elevation, latitude, plant species number, and lizard species number, but corresponds with mainland distance (Table 9; Power 1972). Mainland distance could have affected colonization sequence, which may be reflected in the electrophoretic data. However, for at least scalation, body size, and clutch size, it is likely that the observed pattern of variation is related to climatic factors which are correlated with mainland distance. Other studies have demonstrated that with island area there is a significant negative correlation for dorsal scale number and body size in Uta (Soule 1966), and significant positive correlations for both phenetic and genetic variability in Uta (Soule 1972, Soule and Yang 1973) and in Rattus (Patton et al. 1975). None of these parameters appears correlated with island area in our data; plausible explanations for this include the small number of islands, the relatively near-shore position of the islands, the recency of colonization, and possible differences in response to environmental variables related to the secretive lifestyle of xantusiids.

Evolution and Biogeography On the basis of correlations between electrophoretic data, immunological distance, and the fossil record, Sarich (1977) has estimated that a genetic distance of 1.0 (Nei 1972) indicates a divergence time of approximately 18 million (m.y.) ago. This correlation would predict that Xantusia riversiana diverged from X. henshawi about 15 m.y. ago (middle Miocene) and fromX. vigilis about 10 m.y. ago (late to middle Miocene), while the divergence time between the two mainland species would be approximately 7 m.y. ago (late Miocene). Schatzinger (1975) has recognized two species of Paleoxantusia from the later Eocene (Uintan) of the San Diego region, the larger one sharing characters withX. riversiana and the smaller one with X. henshawi and X. vigilis. The presence of these Paleoxantusia species in the Uintan would seem to suggest that the cladistic event that led to X. riversiana and X. henshawi-vigilis took place over 40 m.y. ago. However, after extensive comparisons among fossil and recent xantusiids, Schatzinger (1975, fig. 9) concluded that these two Paleoxantusia species do not represent the divergence between X. riversiana (Klauherina) and X. henshawi- vigilis (Xantusia), which he feels took place in the Oligocene or later. Our divergence time estimates based on electrophoretic data support his conclusion. The genetic distances between the island populations are extremely small compared with those between the species, indicating that at least two, if not all three, of the present island populations are the result of colonization in the last million years. One of the three could conceivably have been in existence for 10 to 14 m.y., the divergence time between X. riversiana and its living mainland relatives. r. 1.. BEZY ET AL 579

The electrophoretic data appear consistent with the known geological record of the islands (as summarized by J. Vedder, pers. comm.). Pleistocene marine deposits occur on all three islands. On San Nicolas, these are found to the highest present elevation (253 m) and have been estimated to be 0.5 to 0.6 m.y. old. Pleistocene beds that are probably marine cover the highest point (194 m) on Santa Barbara Island, and fossiliferous marine beds occur at the next lower terrace. On San Clemente Island, however, the record of Pleistocene submergence is not as complete. Pleistocene marine beds and wave-cut terraces occur to an elevation of approxi- mately 450m, leaving 149 m without a conclusive record of submergence. Miocene and Pliocene marine beds also occur on San Clemente. While the geological history of the California borderland is highly complex, the evidence would seem to indicate that the coloniza- tions of San Nicolas and Santa Barbara must have been Quaternary events, while it is possible that colonization on San Clemente dates from the late . The occurrence of X. riversiana on islands with records of Pleistocene submergence which were not connected by land bridges suggests that the species is at least a moderately effective island colonizer. The recent discovery of the species on Sutil Island off the north end of Santa Barbara Island (R. Wilson, pers. comm.) strengthens this idea. In contrast, X. vigilis occurs on none of the islands of the Gulf of California, in spite of its circumgulf distribution, and appears to lack all of the life history attributes that are correlated with successful Gulf island coloniza- tion among species of lizards, i.e., habitat generalists having high mainland population densities, potentially high birth rates, and high death rates (Case 1975). The differences in apparent colonizing abilities between the two species seem consistent with what is known of their ecology and life history. The clutch size of X. riversiana is two to three times that of X. vigilis (Goldberg and Bezy 1974). The diet of X. vigilis consists almost exclusively of , while X. riversiana is a generalist, its diet being about evenly divided between plant and material (Brattstrom 1952). Although Xantusia vigilis achieves high densities in relatively cool situations, such as in the Mojave (Zweifel and Lowe 1966) and at localities in Baja California receiving Pacific breezes, it is virtually absent from the hot Gulf coast of Sonora and Baja California (Bezy, pers. obs.). That it does not occur on the Gulf islands is not surprising. While X. riversiana no longer occurs on the mainland, its fossil relatives (Paleoxantusia) appear to have had a long association with the maritime climates of the California borderland (Schatzinger 1975), and today the species reaches high population densities on at least San Clemente Island (Wilson 1976). It is probably the dif- ferences in climate, rather than population parameters, that explain the absence ofX. vigilis on the Gulf islands and the presence of X. riversiana on the California Channel Islands. One of the more interesting unanswered (and perhaps unanswerable) questions posed by X. riversiana is why it does not occur today on the mainland or on other California Islands. Insular shielding from competition, (Savage 1967), and harsh climatic factors (Regal 1968) have all been suggested, and with good reason. Compared with X. henshawi and X. vigilis, the species is morphologically unspecialized (Savage 1967) and its large body size limits its habitat and thermoregulatory options (Regal 1968). Ail three islands lack as potential predators (Savage 1967), two have no other native lizard species, and San Clemente has only Uta stansburiana. (Records for Ula stansburiana [Savage 1967) and mul- ticarinatus [Banta and Wilson 1976] on San Nicolas probably represent introductions.) However, competition may not have played an important role in the elimination ot X. riversiana from the mainland or islands since no other extensively herbivorous lizard is known from the California borderland, at least for the Quaternary. The secretive habits of the species would be expected to minimize predation, except by snakes, and it seems unlikely that predation from this source alone could have been a large factor in bringing about extinction. It 580 ISLAND NIGHT LIZARD DIVERGENCE

would appear more reasonable that climatic change has played the dominant role in producing the relictual biogeographic pattern exhibited by several xantusiids, including X. riversiana (Bezy 1972). The species has probably persisted on the islands primarily because the greater equability of climate there has offered a substantial buffer against the climatic deteriorations of the Neogene. Among the California Islands, the outer, southern ones would be expected to offer the maximum climatic buffer, and it is to these that X. riversiuna is restricted. That the mainland extinction of the species may have occurred more than one million years ago is suggested by the general fossil record for mainland North America (north of the Isthmus of Tehuantepec), which indicates virtually no extinction of lizard species since Blancan times (Gehlbach 1965). In summary, the available evidence suggests that the divergence between Xantusia river- siana and X. henshawi-vigilis took place in the Miocene. Xantusia riversiana could have occurred on San Clemente Island as early as the late Miocene or Pliocene, and its disappearance from the mainland may date to pre-Nebraskan times. In the last half million years or so the species has reached San Nicolas and Santa Barbara Islands, perhaps from San Clemente Island, and the resultant populations have become differentiated in scalation, coloration, body size, and clutch size.

SPECIMENS EXAMINED Catalogue numbers refer to specimens in the collections of the Los Angeles County Museum of Natural History (acronym, LACM, omitted), the Museum of Zoology (MVZ), and the San Diego Natural History Museum (SDNHM). All localities are in California. Santa Barbara Island is in Santa Barbara County, San Clemente Island in Los Angeles County, and San Nicolas Island in Ventura County. (A) Electrophoresis. X. henshawi: RIVERSIDE CO.: ca. 1.3 mi (by road) S Cabezon, 125524-29. X. vigilis: LOS ANGELES CO.: 3.5 mi (airline) W Littlerock, 125530-49. X. riversiana: SANTA BARBARA I.: vie. Cat Canyon, 125463-67. SAN CLEMENTE I.: vie. dunes, NW side of I., 125470-83, 125506-10; 4.8 mi (airline) SE Wilson Cove, 125468; Horse Cove, 125469. SAN NICOLAS I.: Carrier Cove, SE of W Point, 125486-505; beach along SSE side of I., 125512. (B) Karyotypes. SANTA BARBARA I.: vie. Cat Canyon, 125465. SAN NICOLAS I.: beach along SSE side of 1., 127506. (C) Scalation. SANTA BARBARA 1.: 3278-85, 3287-88, MVZ 644-45, MVZ 28330, SDNHM 21128, SDNHM 31983-85, SDNHM 44469; vie. Cat Canyon, 108822-38, 125463- 67. SAN CLEMENTE I.: NW Sample, vie. airport, 108306, 108309-11, 108315, 108319-20, 108322-23, 108327, 108330, 108336, 108347, 108352-56, 108359, 108362-63, 108371-72, 108446, 108449, 108451, 108455-56, 108459, 108462-64, 108470,108473,108483-84,108486-89, 108495-97,108499-500, 108504, 108563, 108577, 108588, 108618, 108620, 108646, 108654, 108678, 108709, 108734, 108739. Pyramid Cove Sample, 3309, 3317, 3330, 3368-69, 3371, 3373, 3377-81, 3383, 3387, 3389-90, 3392-94, 3401. General Sample, Mt. Thirst, 119174; Middle Ranch, 26798; Horse CoVe, 125469; ca. 3 mi W Pyramid Cove, 108607-16; 4 mi S Wilson Cove, 101255-59; 5 mi E Wilson Cove, 101254; 4.8 mi (airline) SE Wilson Cove, 125468. SAN NICOLAS 1. : SE Sample, 108769-74, 108777-88, 108791, 108793-800, 108802, 108804-09, 108811-12, 108818, 125512-14. Carrier Cove

\ R. L. BEZY ET Al. 581

Sample, SE of W Point, 121670-71, 122572, 125486-94, 125496, 125498, 125501- 05, 125511. General Sample, 3267, 14487, 101262, SDNHM 15487-92, SDNHM 15494-5, SDNHM 17213, SDNHM 17215, SDNHM 36334, SDNHM 36670-71; Army Camp, 3266; Sand Dunes, 3275-77.

SUMMARY Xantusia (Klauberina) riversiana is endemic to Santa Barbara, San Clemente, and San Nicolas Islands. Electrophoretic analyses of encoded by 22 to 30 presumptive loci indicate that the genetic distances between the island populations are minute (ND = 0.0004 to 0.0048), compared with those between the species of Xantusia (0.409 to 0.830), and that the heterozygosity levels are low in all the populations (H = 1.80). The unbanded karyotypes of the three island populations appear identical to each other and to those of certain populations of both mainland species. Stepwise discriminant analysis of seven characters demonstrates both intra-island and inter-island divergence in scalation, with an average of 85 per cent of the specimens being correctly assigned to their home island. The island populations have also diverged in coloration, body size, and clutch size. Electrophoretic data suggest that the divergence time between X. riversiana and X. henshawi-vigilis is 10 to 15 m.y. ago (ca. middle Miocene), while that between the island populations is less than one m.y. ago. Xantusia riversiana could have occurred on San Clemente Island from as early as the Miocene or Pliocene and its disappearance from the mainland may date from pre-Nebraskan time.

ACKNOWLEDGMENTS We thank W. G. Kay and W. S. Myers of the U.S. Department of the Navy, W. H. Ehorn of the U.S. Department of the Interior, and J. M. Brode and K. Bali of the California Department of Fish and Game for issuing collecting permits and/or granting access to the islands; K. Bolles, M. A. Recht, M. G. Ruggles, and J. W. Wright for assistance in collecting specimens; D. B. Wake (MVZ) and T. Fritts (formerly SDNHM) for the loan of specimens under their charge; R. D. Friesen for assistance and advice on data analysis; K. Bolles for preparing illustrations; and J. W. Wright and F. S. Truxal for critically reviewing the manuscript.

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